Abstract

Forested ecosystems diversified more than 350 Ma to become major engines of continental silicate weathering, regulating the Earth's atmospheric carbon dioxide concentration by driving calcium export into ocean carbonates. Our field experiments with mature trees demonstrate intensification of this weathering engine as tree lineages diversified in concert with their symbiotic mycorrhizal fungi. Preferential hyphal colonization of the calcium silicate-bearing rock, basalt, progressively increased with advancement from arbuscular mycorrhizal (AM) to later, independently evolved ectomycorrhizal (EM) fungi, and from gymnosperm to angiosperm hosts with both fungal groups. This led to ‘trenching’ of silicate mineral surfaces by AM and EM fungi, with EM gymnosperms and angiosperms releasing calcium from basalt at twice the rate of AM gymnosperms. Our findings indicate mycorrhiza-driven weathering may have originated hundreds of millions of years earlier than previously recognized and subsequently intensified with the evolution of trees and mycorrhizas to affect the Earth's long-term CO2 and climate history.

1. Introduction

Forested ecosystems are major engines of biological weathering in terrestrial environments, but we know almost nothing about how the strength of these engines changed as tree lineages and their root-associating fungal symbionts evolved. Fossil roots of early gymnosperms from at least the Carboniferous are colonized by arbuscular mycorrhizal (AM) fungi, and this type of mycorrhiza continues to be found in the vast majority of tree species, including in most of the more recently evolved angiosperm taxa [1]. Independently evolving ectomycorrhizal (EM) fungi diversified from the Cretaceous, forming mycorrhizal associations with the Pinaceae and angiosperm trees in the Betulaceae and Fagaceae that now dominate temperate and boreal forests, as well as with angiosperm trees in the Myrtaceae, Fabaceae and Dipterocarpaceae, that can form dominant stands in warm temperate and tropical regions [1,2]. Both mycorrhizal types use host photosynthate to support extensive hyphal networks with high absorptive surface area for nutrient element mass transfer from the substrate. In trees forming AM, root functioning is augmented by the nutrient-scavenging activities of the fungi, whereas EM fungi completely envelop tree root tips to subsume the soil–root interface. EM fungi thereby control the translocation of elements from soil to tree and can also enhance mineral weathering through exudation of low molecular weight organic compounds [3,4].

Here, we address the primary hypothesis that functional differences between mycorrhizal types, coupled with the evolution of their host trees, drives intensification of silicate weathering. We used mature tree taxa with crown diversification ages ranging from tens to hundreds of millions of years (figure 1a and table 1) in conjunction with a suite of methods isolating mycorrhizal hyphal effects on mineral weathering by excluding tree roots with mesh bags [8]. The extant gymnosperm taxa available for these studies may be only approximate representatives of the ancestral taxa that dominated temperate forests before the rise to dominance of angiosperms [6,9]. Stem- and crown-node ages estimated with molecular clocks suggest gymnosperms evolved and adapted over the same evolutionary time span as their sister lineages, the angiosperms (table 1) [6]. Mycorrhiza-driven weathering was quantified by burying uniform-sized grains of silicate rocks that are either calcium-rich (basalt) or -poor (granite), along with quartz controls (see the electronic supplementary material, tables S1 and S2). Weathering of calcium from silicates plays a major role in regulating atmospheric CO2 on geological timescales [10,11] by promoting the deposition of marine calcium carbonates. Our field studies control for climate and soil type by focusing on established trees with natural populations of soil micro-organisms at the National Arboretum, Westonbirt, UK.

Sequential chemical extraction of different physico-chemical fractions of the basalt grains provides evidence for the ability of the five major tree–mycorrhiza partnerships (table 1) to mobilize calcium bound within dominant silicates and trace carbonates relative to unweathered controls. The primary calcium sources in basalt are the dominant silicate minerals such as plagioclase. Given minor oxide minerals in the basalt are likely to be iron-bearing oxides, like magnetite that lack calcium, calcium extracted following removal of trace carbonates represents mobilization of silicate-bound calcium into the oxide extraction phase. Calcium dissolution from the oxide and carbonate fractions significantly increased (p < 0.0001) beneath EM-angiosperm compared with AM-gymnosperm trees (table 2), consistent with more extensive basalt colonization and surface alteration of silicates by EM hyphae (figure 2f). Ratios of Ca : Sr (µmol : µmol) aid diagnosis of the Ca source from the different mineral components of basalt, with low ratios in plagioclase (less than 200) [13], the dominant calcium-bearing silicate mineral phase in the basalt, and high ratios in carbonates (more than 500) [14]. The chemical extractions demonstrate that Ca : Sr from the oxide fraction is an order-of-magnitude lower than from carbonates (table 2), indicating calcium extracted from the oxide fraction during hyphal–basalt interactions was predominantly mobilized from plagioclase.

Our experiments with established trees support the hypothesis that both AM and EM fungi direct carbon from plant photosynthesis at silicate rocks containing the highest concentrations of weatherable nutrient elements, and physically degrade mineral surfaces to drive intensification of chemical weathering. This provides the first indication of ‘biosensing’ behaviour by AM fungi, and new field evidence supporting earlier suggestions that EM fungi exhibit similar behaviour based largely on controlled-environment laboratory experiments [12,15]. Across our tree–mycorrhiza types, increased hyphal colonization translates into enhanced basalt weathering (figure 1b and table 2). The observation that AM fungi actively weather minerals challenges the recent assumption that they are passive components of the Earth's biological weathering engine [16]. Moreover, it extends the likely importance of mycorrhiza-driven weathering back to the origins of early forests more than 350 Ma, or even to the rise of the first AM-forming land plants more than 50 Myr earlier than this. Our findings provide empirical support for the hypothesis that the Earth's biological weathering engine may have intensified over evolutionary time, while being regulated by the effects of variations in atmospheric CO2 and climate. Both control forest productivity, nutrient demand and delivery of photosynthate to roots and mycorrhizas that drive global biotic weathering [17].

Acknowledgments

We thank Simon Toomer for permission to use Westonbirt Arboretum, and CEMEX UK Materials Ltd for providing pink Shap granite. We acknowledge NERC award, NE/E015190/1, with tied studentship for J.Q. and NERC/World Universities Network Weathering Consortium award, NE/C521001/1. D.J.B. gratefully acknowledges VSI funding from the University of Sheffield, and additional support through a Royal Society-Wolfson Research Merit Award.

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